Skip to main content
Log in

Side effects of some insecticides on numerical response of Cryptolameus montrouzieri to Dactylopius opuntiae

  • Published:
Phytoparasitica Aims and scope Submit manuscript

Abstract

In recent years, Dactylopius opuntiae (Cockerell) (Hemiptera: Dactylopiidae) has become an increasing threat to the cultivation of prickly pear crops in Morocco. To control this harmful insect scale pest, biological control is usually accompanied by chemical control applications. In this context, the use of some insecticides can alter the numerical response of beneficial organisms (predators) associated with this cochineal. In this study, we investigated the effect of the residues of some insecticides «(d-limonene (60 g/L) applied at 100 mL/hL, mineral oil (780 g/L) at 2000 mL/hL, potassium salts of fatty acid (500 g/L) at 40 mL/hL, pyriproxyfen (100 g/L) at 25 mL/hL, and potassium salts of fatty acid (C7-C18) (500 g/L) at 300 mL/hL)» on the numerical response of Cryptolameus montrouzieri (Mulsant) (Coleoptera: Coccinellidae) feeding on D. opuntiae females under laboratory conditions. The sublethal concentration residues of all tested insecticides did not have lethal effects on Cryptolaemus montrouzieri females. D-limonene (Efficiency of Conversion of Ingested food (E.C.I) = 1371.85), mineral oil (E.C.I = 1383.06), potassium salts of fatty acid (E.C.I = 1583.24), and pyriproxyfen (E.C.I = 987.13) were the most compatible with the predator C. montrouzieri, as they did not significantly affect the number of eggs laid by the females compared to the untreated control. Potassium salt of fatty acid (C7–C18) (500 g/L) (E.C.I = 905.93) was the least compatible with C. montrouzieri, as it led to a significant reduction in the number of eggs laid by predatory females.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Data availability

Not applicable.

References

  • Adalma-Aguilera, C., Llanderal-Cãzares, C., Soto-Hernández, M., & Castillo-Márquez, L. E. (2005). Producción de granacochinilla (Dactylopius coccus Costa) em plantas de nopal a la intempérie y em microtúneles. Agrociencia, 39, 161–171.

    Google Scholar 

  • Agarwala, B. K., & Bardhanroy, P. (1997). Oviposition behavior and reproduction efficiency in ladybeetles (Coccinellidae: Coleoptera). A case study of Menochilus sexmaculata (Fabricus). Journal of Aphidology, 11, 49–59.

    Google Scholar 

  • Agarwala, B. K., & Bardhanroy, P. (1999). Numerical response of ladybird beetles (Coccinellidae: Coleoptera) to aphid prey (Homoptera: Aphididae) in a field bean in Northeast India. Journal of Applied Entomology, 123, 401–405.

    Article  Google Scholar 

  • Ambrose, D. P., Rajan, S. J., & Raja, J. M. (2010). Impacts of Synergy-505 on the functional response and behavior of the reduviid bug, Rhynocoris marginatus. Journal of Insect Science, 10(1), 187. https://doi.org/10.1673/031.010.18701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anjitha, A., Krishnamoorthy, S. V., & Kuttalam, S. (2013). Toxicity of insecticides to the coccinellid predators, Cryptolaemus montrouzieri Mulsant and Scymnus coccivora Ayyar of papaya mealybug, Paracoccus marginatus Williams and Granara de Willink. Journal of Biological Control, 27(1), 18–23.

    Google Scholar 

  • Barbosa, P. R. R., Oliveira, M. D., Giorgi, J. A., Silva-Torres, C. S. A., & Torres, J. B. (2014). Predatory behavior and life history of Tenuisvalvae notata (Coleoptera: Coccinellidae) under variable prey availability conditions. The Fla Entomol, 97, 1026–1034.

    Article  Google Scholar 

  • Baskaran, R. K. M., Lakshmi, L. G., & Uthamasamy, S. (1999). Comparative biology and predatory potential of Australian ladybird beetle (Cryptolaemus montrouzieri) on Planococcus citri and Dactylopius tomentosus. Indian Journal of Agricultural Sciences, 69, 605–606.

    Google Scholar 

  • Baumgärtner, J., Bieri, M., & Delucchi, V. (1987). Growth and development of immature life stages of Propylea 14 punctata L. and Coccinella 7-punctata L. (Coleoptera: Coccinellidae) simulated by the metabolic pool model. Entomophaga, 32, 415–423.

    Article  Google Scholar 

  • Bouharroud, R., Amarraque, A., & Qessaoui, R. (2016). First report of the Opuntia Cochineal scale Dactylopius opuntiae (Hemiptera : Dactylopiidae) in Morocco. EPPO Bull, 46(2), 308–310.

    Article  Google Scholar 

  • Brennan, T. C. R., Kromer, J. O., & Nielsen, L. K. (2013). Physiological and transcriptional responses of Saccharomyces cerevisiae to d-limonene show changes to the cell wall but not to the plasma membrane. Appl Environ Microbiol, 79, 3590–3600.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Candolfi, M. P., Barrett, K. L., Campbell, P., Forster, R., Grandy, N., & Huet, M. C. (2001). Guidance document on regulatory testing and risk assessment procedures for plant protection products with non-target arthropods. European standard characteristics of regulatory testing (ESCORT 2) workshop (pp. 21–23). SETAC Europe.

    Google Scholar 

  • Carver, R. H., & Nash, J. G. (2011). Doing data analysis with SPSS: Version 18.0. Cengage Learning.

    Google Scholar 

  • Castro, R. M., Barros, R., Paranhos, B. A., Gava, C. A., Fernandes, M. H., Garziera, L., Siqueira, M. C. (2012). Exigências térmicas de Zagreus bimaculosus (Mulsant) (Coleoptera : Coccinellidae). In Embrapa Semiárido-Resumo em anais de congresso (ALICE). In: CONGRESSO BRASILEIRO DE ENTOMOLOGIA, 14., 2012, Curitiba. SEB-40 anos de avanços da Ciência Entomológica Brasileira. Curitiba: SEB, 2012.

  • Chong, J. H., & Oetting, R. D. (2006). Functional response and progeny production of the Madeira mealybug parasitoid, Anagyrus sp. nov. nr. sinope: The effects of host and parasitoid densities. Biological Control, 39, 320–328.

    Article  Google Scholar 

  • Cranshaw, W. S., Baxendale, B. (2011). Insect Control: Horticultural Oils. Colorado State Univirsity, http://www.ext.colostate.edu/pubs/insect/05569.html. Accessed 3 May 2017.

  • El Aalaoui, M., & Sbaghi, M. (2022). Effects of sublethal concentrations of some biorational insecticides in predation potential of Cryptolaemus montrouzieri on Dactylopius opuntiae. International Journal of Tropical Insect Science, 42(1), 519–526.

    Article  Google Scholar 

  • El Aalaoui, M., Bouharroud, R., Sbaghi, M., El Bouhssini, M., Hilali, L., & Dari, K. (2019). Comparative toxicity of different chemical and biological insecticides against the scale insect Dactylopius opuntiae and their side effects on the predator Cryptolaemus montrouzieri. Archives of Phytopathology and Plant Protection, 52(1-2), 155–169.

    Article  Google Scholar 

  • El Aalaoui, M., Bouharroud, R., Sbaghi, M., El Bouhssini, M., & Hilali, L. (2020). Functional response and predation potential of Hyperaspis campestris (Herbst 1783)(Coleoptera: Coccinellidae) on Opuntiae Cochineal Dactylopius opuntiae (Hemiptera: Dactylopiidae) in Morocco. Test Engineering & Management, 82, 5976–5985.

    Google Scholar 

  • Evans, E. W., & Dixon, A. F. G. (1986). Cues for oviposition by ladybird beetles (Coccinellidae): Response to aphids. The Journal of Animal Ecology, 55, 1027–1034.

    Article  Google Scholar 

  • Giorgi, J. A., Barbosa, P. R. R., Oliveira, J. E. M., & Torres, J. B. (2017). Prodiloides bipunctata Weise (Coccinellidae : Cephaloscymnini): New research on native natural predators of the carmine cochineal, Dactylopius opuntiae (cockerel) (Hemiptera: Dactylopiidae) in the Brazilian semi-arid. The Coleopterists Bulletin, 72(3), 562–564.

    Article  Google Scholar 

  • Halappa, B., Awaknavar, J. S., Archana, D., Bandi, S., & Kumar, G. A. (2013). Laboratory evaluation of insecticides against australian beetle, Cryptolaemus montrouzieri Mulsant (Coccinellidae: Coleoptera). Current Biotica, 7(3), 196–201.

    Google Scholar 

  • He, Y., Zhao, J., Zheng, Y., Desneux, N., & Wu, K. (2012). Lethal effect of imidacloprid on the coccinellid predator Serangium japonicum and sublethal effects on predator voracity and on functional response to the whitefly Bemisia tabaci. Ecotoxicol, 21(5), 1291–1300.

    Article  CAS  Google Scholar 

  • Helmy, E. I., Kwaiz, F. A., & El-Sahn, O. M. N. (2012). The usage of mineral oils to control insects. Egyptian Academic Journal of Biological Sciences (A. Entomology), 5(3), 167–174.

    Article  Google Scholar 

  • Hodek, I., & Honek, A. (1996). Ecology of Coccinellidae (p. 464). Kluwer Academic Publishers.

    Book  Google Scholar 

  • Holling, C. S. (1959). Some characteristics of simple types of predation and parasitism. Canadian Entomologist, 91, 385–398.

    Article  Google Scholar 

  • Karr L. L. (1989). Toxic properties of d-limonene in insects and the earthworm Eisenia fetida. Dissertations, University of Iowa, Ames, IA (US).

  • Khan, H. A. A., Sayyed, A. H., Akram, W., Raza, S., & Ali, M. (2012). The predatory potential of Chrysoperla carnea and Cryptolaemus montrouzieri larvae on different stages of the mealybug, Phenacoccus solenopsis: A threat to cotton in South Asia. Journal of Insect Science, 12, 147.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li, D. X., Tian, J., & Shen, Z. R. (2006). Effects of pesticides on the functional response of predatory thrips, Scolothrips takahashii to Tetranychus viennensis. Journal of Applied Entomology, 130(5), 314–322.

    Article  CAS  Google Scholar 

  • Lima, M. S., Silva, M. P., Ferreira, W. M., Silva, L. D., & Paranhos, B. A. J. (2011). Predadores associados a Dactylopius opuntiae (Hemiptera: Dactylopiidae) em palma forrageira no estado de Pernambuco, Brasil. Revista Chilena de Entomologia, 36, 51–54.

    Google Scholar 

  • Mahmoudi, M., Sahragard, A., & Jalali Sendi, J. (2010). Foraging efficiency of Lysiphlebus fabarum Marshall (Hymenoptera: Aphidiidae) parasitizing the black bean aphid, Aphis fabae Scopoli (Hemiptera: Aphididae), under laboratory conditions. Journal of Asia-Pacific Entomology, 13, 111–116.

    Article  Google Scholar 

  • Malaquias, J. B., Ramalho, F. S., Omoto, C., Godoy, W. A. C., & Silveira, R. F. (2014). Imidacloprid affects the functional response of predator Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) to strains of Spodoptera frugiperda (J.E. Smith) on Bt cotton. Ecotoxicol, 23, 192–200.

    Article  CAS  Google Scholar 

  • Martinou, A. F., & Stavrinides, M. C. (2015). Effects of sublethal concentrations of insecticides on the functional response of two Mirid generalist predators. PLoS One, 10(12), e0144413.

    Article  PubMed  PubMed Central  Google Scholar 

  • Martinou, A. F., Raymond, B., Milonas, P. G., & Wright, D. J. (2010). Impact of intraguild predation on parasitoid foraging behaviour. Ecological Entomology, 35, 183–189.

    Article  Google Scholar 

  • Mendel, Z., Protasov, A., Carvalho, C.J., Vanegas, J.M., Refugio Lomeli, F., Refugio Leyva, E. (2018). Biological control possibilities of an invasive scale insect in Israel: opuntia cochineal scale insect Dactylopius opuntiae. In XI European Congress of Entomology, Book of Abstracts (p. 40). 2–6 July 2018, Napoli, Italy.

  • Nawaz, M., Cai, W., Jing, Z., Zhou, X., Mabubu, J. I., & Hua, H. (2017). Toxicity and sublethal effects of chlorantraniliprole on the development and fecundity of a non-specific predator, the multicolored Asian lady beetle, Harmonia axyridis (Pallas). Chemosphere, 178, 496–503.

    Article  CAS  PubMed  Google Scholar 

  • Ofuya, T. I., & Akingbohungbe, A. E. (1988). Functional and numerical responses of Cheilomenes lunata (Fabricius) (Coleoptera: Coccinellidae) feeding on cowpea aphid, Aphis craccivora Koch (Homoptera: Aphididae). International Journal of Tropical Insect Science, 9(4), 543–546.

    Article  Google Scholar 

  • Omkar, & Pervez, A. (2004). Functional and numerical responses of Propylea dissecta (Mulsant) (Col., Coccinellidae). Journal of Applied Entomology, 128, 140–146.

    Article  Google Scholar 

  • Planes, L., Catalán, J., Tena, A., Porcuna, J. L., Jacas, J. A., Izquierdo, J., & Urbaneja, A. (2013). Lethal and sublethal effects of spirotetramat on the mealybug destroyer, Cryptolaemus montrouzieri. Journal of Pest Science, 86(2), 321–327.

    Article  Google Scholar 

  • Protasov, A., Mendel, Z., Spodek, M., & Carvalho, C. J. (2017). Management of the Opuntia cochineal scale insect, Dactylopius opuntiae (Cockerell) in Israel. Alon Hanotea, 71, 48–51.

    Google Scholar 

  • Rimoldi, F., Fogel, M. N., Ronco, A. E., & Schneider, M. I. (2017). Comparative susceptibility of two Neotropical predators, Eriopis connexa and Chrysoperla externa, to acetamiprid and pyriproxyfen: Short and long-term effects after egg exposure. Environmental Pollution, 231, 1042–1050.

    Article  CAS  PubMed  Google Scholar 

  • Sabaghi, R., Hosseini, R., & Sahragard, A. (2011). Functional and numerical responses of Scymnus Syriacus Marseul (Coleoptera: Coccinellidae) to the black bean aphid, Aphis Fabae Scopoli (Hemiptera: Aphididae) under laboratory conditions. Journal of Plant Protection Research, 51, 423–428.

    Article  Google Scholar 

  • Sahito, H. A., Abro, G. H., Syed, T. S., Memon, S. A., Mal, B., & Kaleri, S. (2011). Screening of pesticides against cotton mealybug Phenacoccus solenopsis Tinsley and its natural enemies on cotton crop. International Research Journal of Biochemistry and Bioinformatics, 19, 232–236.

    Google Scholar 

  • Sanches N. F., & Carvalho R. S. (2010). Procedimentos para manejo da criação e multiplicação do predador exótico Cryptolaemus montrouzieri. Cruz dasAlmas: BrasilEmbrapa Mandioca e Fruticultura (Circular Técnica, 99).

  • Solomon, M. E. (1949). The natural control of animal populations. The Journal of Animal Ecology, 18, 1–35.

    Article  Google Scholar 

  • Sullivan, J. J., & Goh, K. S. (2008). Environmental fate and properties of pyriproxyfen. Journal of Pesticide Science, 33(4), 339–350.

    Article  CAS  Google Scholar 

  • Taylor, W. E., & Vickery, B. (1974). Insecticidal properties of limonene, a constituent of citrus oil. Ghana Journal of Agricultural Science, 7, 61–62.

    Google Scholar 

  • Tsolakis, H., & Ragusa, S. (2008). Effects of a mixture of vegetable and essential oils and fatty acid potassium salts on Tetranychus urticae and Phytoseiulus persimilis. Ecotoxicology and Environmental Safety, 70(2), 276–282.

    Article  CAS  PubMed  Google Scholar 

  • Uygun, N., & Atlihan, R. (2000). The effect of temperature on development and fecundity of Scymnus levaillanti. BioControl, 45, 453–462.

    Article  Google Scholar 

  • Vanegas-Rico, J. M., Lomeli-Flores, J. R., Rodríguez-Leyva, E., Mora-Aguilera, G., & Valdez, J. M. (2010). Natural enemies of Dactylopius opuntiae (Cockerell) on Opuntia ficus-indica (L.) Miller in Central Mexico. Acta Zoológica Mexicana, 26, 415–433.

    Article  Google Scholar 

  • Vanegas-Rico, J. M., Rodríguez-Leyva, E., Lomeli-Flores, J. R., González-Hernández, H., Pérez-Panduro, A., & MoraAguilera, G. (2016). Biology and life history of Hyperaspis trifurcate feeding on Dactylopius opuntiae. BioControl, 61, 691–701.

    Article  Google Scholar 

  • Wanumen, A. C., Sánchez-Ramos, I., Viñuela, E., Medina, P., & Adán, Á. (2016). Impact of feeding on contaminated prey on the life parameters of Nesidiocoris tenuis (Hemiptera: Miridae) adults. Journal of Insect Science, 16(1), 103. https://doi.org/10.1093/jisesa/iew084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wright, E. J., & Laing, J. E. (1980). Numerical response of Coccinellids to aphids in corn in southern Ontario. Canadian Entomologist, 112, 977–988.

    Article  Google Scholar 

  • Xiao, D., Zhao, J., Guo, X., Chen, H., Qu, M., Zhai, W., Desneux, N., Biondi, A., Zhang, F., & Wang, S. (2016). Sublethal effects of imidacloprid on the predatory seven-spot ladybird beetle Coccinella septempunctata. Ecotoxicol, 25(10), 1782–1793.

    Article  CAS  Google Scholar 

  • Yousef-Yousef, M., & Quesada-Moraga, E. (2020). Towards Dactylopius opuntiae (Cockerell) (Hemiptera : Dactylopiidae) biological and integrated management at field conditions in Cadiz province (Spain). Biocontrol Science and Technology, 30(9), 951–961.

    Article  Google Scholar 

Download references

Funding

The research of this study was supported by the National Institute of Agricultural Research (INRA), Morocco.

Author information

Authors and Affiliations

Authors

Contributions

Mohamed El Aalaoui. conceptualization, methodology, formal analysis, prepared figures, and wrote the main manuscript text; Mohamed Sbaghi. supervision, visualization, and review of the article. All authors reviewed the manuscript.

Corresponding author

Correspondence to Mohamed El Aalaoui.

Ethics declarations

Ethics approval and consent to participate

This article does not contain any studies with human participants or animals performed by any of the authors.

Consent for publication

Not applicable.

Conflict of interest

The authors declare that they have no conflict of interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El Aalaoui, M., Sbaghi, M. Side effects of some insecticides on numerical response of Cryptolameus montrouzieri to Dactylopius opuntiae. Phytoparasitica 51, 513–520 (2023). https://doi.org/10.1007/s12600-023-01073-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12600-023-01073-y

Keywords

Navigation